Photochemical attributes determine the responses of plant species from different functional groups of ferruginous outcrops when grown in iron mining substrates
Camilla Oliveira Rios
A , Paulo Antônio Pimentel B , Elisa Monteze Bicalho C , Queila Souza Garcia D and Eduardo Gusmão Pereira B *
A
B
C
D
Abstract
Environments originating from banded iron formations, such as the canga, are important reference ecosystems for the recovery of degraded areas by mining. The objective of this work was to evaluate if the relationship between morphofunctional and photosynthetic attributes of native canga species from different functional group results in distinct responses when grown in iron mining tailings substrate. The experiment was carried out with species belonging to different functional groups: a widespread semi-deciduous tree-shrub, Myrcia splendens; an endemic deciduous shrub, Jacaranda caroba; and a nitrogen-fixing herbaceous species, Periandra mediterranea. The species were grown in two conditions, reference soil and iron ore tailing. Despite belonging to different functional groups when grown in tailings, the morphofunctional attributes presented similar responses between species. M. splendens was the species most affected by the conditions imposed by the iron ore mining tailings, with decreased light-use efficiency and electron transport. P. mediterranea had satisfactory growth and maintenance of photosynthetic attributes. J. caroba growing in the tailings increased the effective quantum yield of PSII. The photochemical and growth assessments were able to better explain the adaptive strategies developed by the species, guaranteeing a greater chance of success during the rehabilitation of mining substrates.
Keywords: canga, chlorophyll a fluorescence, deciduous shrub, ecological restoration, functional groups, native species, nitrogen-fixing, reference ecosystems, widespread semideciduous.
References
Albert CH, Thuiller W, Yoccoz NG, Douzet R, Aubert S, Lavorel S (2010) A multi-trait approach reveals the structure and the relative importance of intra- vs. interspecific variability in plant traits. Functional Ecology 24, 1192-1201.
| Crossref | Google Scholar |
Aslan CE (2019) Implications of non-native species for mutualistic network resistance and resilience. PLoS ONE 14, e0217498.
| Crossref | Google Scholar | PubMed |
Balazs KR, Kramer AT, Munson SM, Talkington N, Still S, Butterfield BJ (2020) The right trait in the right place at the right time: matching traits to environment improves restoration outcomes. Ecological Applications 30, e02110.
| Crossref | Google Scholar | PubMed |
Blondel J (2003) Guilds or functional groups: does it matter? Oikos 100, 223-231.
| Crossref | Google Scholar |
Bremner J, Rogers SI, Frid CLJ (2006) Methods for describing ecological functioning of marine benthic assemblages using biological traits analysis (BTA). Ecological Indicators 6, 609-622.
| Crossref | Google Scholar |
Carvalho PER (2014) ‘Espécies arbóreas brasileiras.’ (Embrapa Informação Tecnológica: Brasília, Brazil). Available at https://www.alice.cnptia.embrapa.br/alice/handle/doc/305634
Castro-Díez P, Puyravaud JP, Cornelissen JHC (2000) Leaf structure and anatomy as related to leaf mass per area variation in seedlings of a wide range of woody plant species and types. Oecologia 124, 476-486.
| Crossref | Google Scholar | PubMed |
Cruz FVdS, Gomes MP, Bicalho EM, Garcia QS (2022) Fertilization assures mineral nutrition but does not overcome the effects of Fe accumulation in plants grown in iron ore tailings. Environmental Science and Pollution Research 29, 18047-18062.
| Crossref | Google Scholar |
da Silva FL, Araújo FGS, Teixeira MP, Gomes RC, von Krüger FL (2014) Study of the recovery and recycling of tailings from the concentration of iron ore for the production of ceramic. Ceramics International 40, 16085-16089.
| Crossref | Google Scholar |
Daughtry CST, Walthall CL, Kim MS, de Colstoun EB, McMurtrey JE, III (2000) Estimating corn leaf chlorophyll concentration from leaf and canopy reflectance. Remote Sensing of Environment 74, 229-239.
| Crossref | Google Scholar |
de Carvalho F, de Souza FA, Carrenho R, Moreira FMdS, Jesus EdC, Fernandes GW (2012) The mosaic of habitats in the high-altitude Brazilian rupestrian fields is a hotspot for arbuscular mycorrhizal fungi. Applied Soil Ecology 52, 9-19.
| Crossref | Google Scholar |
de Castro Pena JC, Goulart F, Wilson Fernandes G, Hoffmann D, Leite FSF, Britto dos Santos N, Soares-Filho B, Sobral-Souza T, Humberto Vancine M, Rodrigues M (2017) Impacts of mining activities on the potential geographic distribution of eastern Brazil mountaintop endemic species. Perspectives in Ecology and Conservation 15, 172-178.
| Crossref | Google Scholar |
de Freitas ADD, Herrera RC, Figueredo FAO, Junior OF, da Costa RCL (2021) Germinação de sementes e morfologia de Jacaranda copaia (Aubl.) D. Don. Biota Amazônia 11, 11-14.
| Google Scholar |
de la Riva EG, Olmo M, Poorter H, Ubera JL, Villar R (2016) Leaf mass per area (LMA) and its relationship with leaf structure and anatomy in 34 Mediterranean woody species along a water availability gradient. PLoS ONE 11, e0148788.
| Crossref | Google Scholar | PubMed |
de Matos LP, de Andrade HM, Marinato CS, de Oliveira Prado IG, Coelho DG, Montoya SG, Kasuya MCM, de Oliveira JA (2020) Limitations to use of Cassia grandis L. in the revegetation of the areas impacted with mining tailings from Fundão Dam. Water, Air, & Soil Pollution 231, 127.
| Crossref | Google Scholar |
Dudley N, Eufemia L, Fleckenstein M, Periago ME, Petersen I, Timmers JF (2020) Grasslands and savannahs in the UN Decade on Ecosystem Restoration. Restoration Ecology 28, 1313-1317.
| Crossref | Google Scholar |
Fernandes GW, Ribeiro SP (2017) Deadly conflicts: mining, people, and conservation. Perspectives in Ecology and Conservation 15, 141-144.
| Crossref | Google Scholar |
Figueiredo MA, Diniz AP, Abreu ATd, Messias MCTB, Kozovits AR (2018) Growing Periandra mediterranea on post-mining substrate: native Fabaceae with potential for revegetation of degraded rupestrian grasslands in Brazil. Acta Botanica Brasilica 32, 232-239.
| Crossref | Google Scholar |
Funch LS, Barroso GM (1999) Revisão taxonômica do gênero Periandra Mart. ex Benth. (Leguminosae, Papilionoideae, Phaseoleae). Brazilian Journal of Botany 22, 539-564.
| Crossref | Google Scholar |
Gagen EJ, Levett A, Paz A, Gastauer M, Caldeira CF, Valadares RBdS, Bitencourt JAP, Alves R, Oliveira G, Siqueira JO, Vasconcelos PM, Southam G (2019) Biogeochemical processes in canga ecosystems: armoring of iron ore against erosion and importance in iron duricrust restoration in Brazil. Ore Geology Reviews 107, 573-586.
| Crossref | Google Scholar |
Gamito S, Patrício J, Neto JM, Teixeira H, Marques JC (2012) Feeding diversity index as complementary information in the assessment of ecological quality status. Ecological Indicators 19, 73-78.
| Crossref | Google Scholar |
Garcia QS, Barreto LC, Bicalho EM (2020) Environmental factors driving seed dormancy and germination in tropical ecosystems: a perspective from campo rupestre species. Environmental and Experimental Botany 178, 104164.
| Crossref | Google Scholar |
Gastauer M, Souza Filho PWM, Ramos SJ, Caldeira CF, Silva JR, Siqueira JO, Furtini Neto AE (2019) Mine land rehabilitation in Brazil: goals and techniques in the context of legal requirements. Ambio 48, 74-88.
| Crossref | Google Scholar | PubMed |
Gastauer M, Sarmento PSdM, Santos VCA, Caldeira CF, Ramos SJ, Teodoro GS, Siqueira JO (2020) Vegetative functional traits guide plant species selection for initial mineland rehabilitation. Ecological Engineering 148, 105763.
| Crossref | Google Scholar |
Gentry AH (1992) Bignoniaceae: part II (tribe Tecomeae). Flora Neotropica 25, 1-370.
| Google Scholar |
Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta (BBA) – General Subjects 990, 87-92.
| Crossref | Google Scholar |
Gibson N, Yates CJ, Dillon R (2010) Plant communities of the ironstone ranges of South Western Australia: hotspots for plant diversity and mineral deposits. Biodiversity and Conservation 19, 3951-3962.
| Crossref | Google Scholar |
Giljum S, Maus V, Kuschnig N, Luckeneder S, Tost M, Sonter LJ, Bebbington AJ (2022) A pantropical assessment of deforestation caused by industrial mining. Proceedings of the National Academy of Sciences 119, e2118273119.
| Crossref | Google Scholar |
Ginocchio R, León-Lobos P, Arellano EC, Anic V, Ovalle JF, Baker AJM (2017) Soil physicochemical factors as environmental filters for spontaneous plant colonization of abandoned tailing dumps. Environmental Science and Pollution Research 24, 13484-13496.
| Crossref | Google Scholar | PubMed |
Guimarães ZTM, dos Santos VAHF, Ferreira MJ (2022) Chlorophyll a fluorescence parameters are related to the leaf economics spectrum of tropical tree species in a mixed plantation. Trees 36, 763-775.
| Crossref | Google Scholar |
He M, Yan Z, Cui X, Gong Y, Li K, Han W (2020) Scaling the leaf nutrient resorption efficiency: nitrogen vs phosphorus in global plants. Science of The Total Environment 729, 138920.
| Crossref | Google Scholar | PubMed |
Holl KD, Brancalion PHS (2020) Tree planting is not a simple solution. Science 368, 580-581.
| Crossref | Google Scholar | PubMed |
Hunt R (1979) Plant growth analysis: the rationale behind the use of the fitted mathematical function. Annals of Botany 43, 245-249.
| Crossref | Google Scholar |
Khurana E, Singh JS (2001) Ecology of seed and seedling growth for conservation and restoration of tropical dry forest: a review. Environmental Conservation 28, 39-52.
| Crossref | Google Scholar |
Kienberg O, Thill L, Baumbach H, Becker T (2014) A method for selecting plant species for reintroduction purposes: a case-study on steppe grassland plants in Thuringia (Germany). Tuexenia 34, 467-488.
| Crossref | Google Scholar |
Kikuzawa K (2003) Phenological and morphological adaptations to the light environment in two woody and two herbaceous plant species. Functional Ecology 17, 29-38.
| Crossref | Google Scholar |
Kikuzawa K, Koyama H, Umeki K, Lechowicz MJ (1996) Some evidence for an adaptive linkage between leaf phenology and shoot architecture in sapling trees. Functional Ecology 10, 252-257.
| Crossref | Google Scholar |
Kikuzawa K, Onoda Y, Wright IJ, Reich PB (2013) Mechanisms underlying global temperature-related patterns in leaf longevity. Global Ecology and Biogeography 22, 982-993.
| Crossref | Google Scholar |
Larsen TH, Williams NM, Kremen C (2005) Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecology Letters 8, 538-547.
| Crossref | Google Scholar | PubMed |
Le Stradic S, Buisson E, Negreiros D, Campagne P, Wilson Fernandes G (2014) The role of native woody species in the restoration of Campos Rupestres in quarries. Applied Vegetation Science 17, 109-120.
| Crossref | Google Scholar |
Le Stradic S, Silveira FAO, Buisson E, Cazelles K, Carvalho V, Fernandes GW (2015) Diversity of germination strategies and seed dormancy in herbaceous species of campo rupestre grasslands. Austral Ecology 40, 537-546.
| Crossref | Google Scholar |
Lohmann LG, Pirani JR (1996) Tecomeae (Bignoniaceae) from the Espinhaço Range, Minas Gerais and Bahia, Brazil. Acta Botanica Brasilica 10, 103-138.
| Crossref | Google Scholar |
Maciel GP, Caldeira CF, Gastauer M, Ribeiro PG, da Silva GM, Ramos SJ (2023) Morphological characteristics and germination of native species seeds for mineland rehabilitation in the Eastern Amazon. New Forests 54, 769-787.
| Crossref | Google Scholar |
Madejón P, Murillo JM, Marañón T, Cabrera F, Soriano M (2003) Trace element and nutrient accumulation in sunflower plants two years after the Aznalcóllar mine spill. Science of The Total Environment 307, 239-257.
| Crossref | Google Scholar | PubMed |
Maguire JD (1962) Speed of germination – aid in selection and evaluation for seedling emergence and vigor. Crop Science 2, 176-177.
| Crossref | Google Scholar |
Malavolta E, Vitti GC, de Oliveira SA (1997) ‘Avaliação do estado nutricional das plantas: princípios e aplicações.’ (Associacşão Brasileira para Pesquisa da Potassa e do Fosfato: Piracicaba, Brazil). Available at https://repositorio.usp.br/item/001070906
Meira RMSA, Peixoto AL, Coelho MAN, Ponzo APL, Esteves VGL, Silva MC, Câmara PEAS, Meira-Neto JAA (2016) Brazil’s mining code under attack: giant mining companies impose unprecedented risk to biodiversity. Biodiversity and Conservation 25, 407-409.
| Crossref | Google Scholar |
Menéndez E, Ramírez-Bahena M-H, Carro L, Fernández-Pascual M, Peter Klenk H, Velázquez E, Mateos PF, Peix A, Rita Scotti M (2016) Paenibacillus periandrae sp. nov., isolated from nodules of Periandra mediterranea. International Journal of Systematic and Evolutionary Microbiology 66, 1838-1843.
| Crossref | Google Scholar | PubMed |
Milberg P, Andersson L, Thompson K (2000) Large-seeded spices are less dependent on light for germination than small-seeded ones. Seed Science Research 10, 99-104.
| Crossref | Google Scholar |
Miola DTB, Ramos VDV, Silveira FAO (2021) A brief history of research in campo rupestre: identifying research priorities and revisiting the geographical distribution of an ancient, widespread Neotropical biome. Biological Journal of the Linnean Society 133, 464-480.
| Crossref | Google Scholar |
Morais PO, Lombardi JA (2006) A família Myrtaceae na reserva particular do patrimônio natural da Serra do Caraça, Catas Altas, Minas Gerais, Brasil. Lundiana: International Journal of Biodiversity 7, 3-32.
| Crossref | Google Scholar |
Navarro-Cano JA, Goberna M, Verdú M (2019) Using plant functional distances to select species for restoration of mining sites. Journal of Applied Ecology 56, 2353-2362.
| Crossref | Google Scholar |
Negreiros D, Fernandes GW, Efremova AA, Le Stradic S, Neves ACO (2016) Growth–survival trade-off in shrub saplings from Neotropical mountain grasslands. South African Journal of Botany 106, 17-22.
| Crossref | Google Scholar |
Nogueira CB, Menéndez E, Ramírez-Bahena MH, Velázquez E, Peix Á, Mateos PF, Scotti MR (2019) The N-fixing legume Periandra mediterranea constrains the invasion of an exotic grass (Melinis minutiflora P. Beauv) by altering soil N cycling. Scientific Reports 9, 11033.
| Crossref | Google Scholar |
Oliveira RS, Galvão HC, de Campos MCR, Eller CB, Pearse SJ, Lambers H (2015) Mineral nutrition of campos rupestres plant species on contrasting nutrient-impoverished soil types. New Phytologist 205, 1183-1194.
| Crossref | Google Scholar | PubMed |
Oliveira-Filho AT, Fontes MAL (2000) Patterns of floristic differentiation among Atlantic Forests in Southeastern Brazil and the influence of climate. Biotropica 32, 793-810.
| Crossref | Google Scholar |
Park S, Kim JH, Byun C, Hong SY, Lee EJ (2021) Identification of restoration species for early roadcut slope regeneration using functional group approach. Restoration Ecology 29, e13424.
| Crossref | Google Scholar |
Pereira PH, Mansano VdF (2008) Estudos taxonômicos da tribo Tecomeae (Bignoniaceae) no Parque Nacional do Itatiaia, Brasil. Rodriguésia 59, 265-289.
| Crossref | Google Scholar |
Poorter H, Remkes C (1990) Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83, 553-559.
| Crossref | Google Scholar | PubMed |
Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist 182, 565-588.
| Crossref | Google Scholar | PubMed |
Poorter L, Castilho CV, Schietti J, Oliveira RS, Costa FRC (2018) Can traits predict individual growth performance? A test in a hyperdiverse tropical forest. New Phytologist 219, 109-121.
| Crossref | Google Scholar | PubMed |
Rios CO (2022) From the field to the recovery of degraded areas: an ecophysiological approach in the selection of native plant species from Banded Iron Formations (BIFs). Available at https://repositorio.ufmg.br/handle/1843/56879
Rios CO, Siqueira-Silva AI, Pereira EG (2021) How does drought affect native grasses’ photosynthesis on the revegetation of iron ore tailings? Environmental Science and Pollution Research 28, 14797-14811.
| Crossref | Google Scholar | PubMed |
Rios CO, Pimentel PA, Živčák M, Brestič M, Pereira EG (2022) Can ecological strategies be explained by photochemical efficiency in ironstone outcrops vegetation? Plant and Soil 480, 105-120.
| Crossref | Google Scholar |
Rios CO, Siqueira-Silva AI, Pereira EG (2023) Revegetation of mining-impacted sites with a tropical native grass: constraints of climate seasonality and trace-element accumulation. Journal of Environmental Management 326, 116655.
| Crossref | Google Scholar | PubMed |
Sancho-Knapik D, Escudero A, Mediavilla S, Scoffoni C, Zailaa J, Cavender-Bares J, Álvarez-Arenas TG, Molins A, Alonso-Forn D, Ferrio JP, Peguero-Pina JJ, Gil-Pelegrín E (2021) Deciduous and evergreen oaks show contrasting adaptive responses in leaf mass per area across environments. New Phytologist 230, 521-534.
| Crossref | Google Scholar | PubMed |
Santos TRS, Santos JAS, Pereira EG, Garcia QS (2023) Revegetation of an area impacted by iron ore tailings: evaluating fertilization alternatives in native pioneer and secondary trees. Environmental Science and Pollution Research 30, 3760-3773.
| Crossref | Google Scholar |
Silva JG, Gomes MP, Pereira EG, Bicalho EM, Garcia QS (2022) Initial growth of Peltophorum dubium is affected by nitrogen source and manganese concentration. Journal of Soil Science and Plant Nutrition 22, 201-211.
| Crossref | Google Scholar |
Silveira FAO, Negreiros D, Barbosa NPU, Buisson E, Carmo FF, Carstensen DW, Conceição AA, Cornelissen TG, Echternacht L, Fernandes GW, Garcia QS, Guerra TJ, Jacobi CM, Lemos-Filho JP, Le Stradic S, Morellato LPC, Neves FS, Oliveira RS, Schaefer CE, Viana PL, Lambers H (2016) Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant and Soil 403, 129-152.
| Crossref | Google Scholar |
Skirycz A, Castilho A, Chaparro C, Carvalho N, Tzotzos G, Siqueira JO (2014) Canga biodiversity, a matter of mining. Frontiers in Plant Science 5, 653.
| Crossref | Google Scholar | PubMed |
Soliveres S, van der Plas F, Manning P, Prati D, Gossner MM, Renner SC, Alt F, Arndt H, Baumgartner V, Binkenstein J, et al. (2016) Biodiversity at multiple trophic levels is needed for ecosystem multifunctionality. Nature 536, 456-459.
| Crossref | Google Scholar | PubMed |
Souza JP, Prado CHBA, Damascos MA, Albino ALS (2009) Influence of shoot inclination on irradiance and morphophysiological leaf traits along shoots in cerrado trees with distinct leaf deciduousness. Brazilian Journal of Plant Physiology 21, 281-289.
| Crossref | Google Scholar |
Stanturf JA, Kleine M, Mansourian S, Parrotta J, Madsen P, Kant P, Burns J, Bolte A (2019) Implementing forest landscape restoration under the Bonn challenge: a systematic approach. Annals of Forest Science 76, 50.
| Crossref | Google Scholar |
Valliere JM, Ruscalleda Alvarez J, Cross AT, Lewandrowski W, Riviera F, Stevens JC, Tomlinson S, Tudor EP, Wong WS, Yong JWH, Veneklaas EJ (2022) Restoration ecophysiology: an ecophysiological approach to improve restoration strategies and outcomes in severely disturbed landscapes. Restoration Ecology 30, e13571.
| Crossref | Google Scholar |
Viana PL, Lombardi JA (2007) Florística e caracterização dos campos rupestres sobre canga na Serra da Calçada, Minas Gerais, Brasil. Rodriguésia 58, 157-177.
| Crossref | Google Scholar |
Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Groom PK, Hikosaka K, Lee W, Lusk CH, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Warton DI, Westoby M (2005) Modulation of leaf economic traits and trait relationships by climate. Global Ecology and Biogeography 14, 411-421.
| Crossref | Google Scholar |
Wright IJ, Dong N, Maire V, Prentice IC, Westoby M, Díaz S, Gallagher RV, Jacobs BF, Kooyman R, Law EA, Leishman MR, Niinemets Ü, Reich PB, Sack L, Villar R, Wang H, Wilf P (2017) Global climatic drivers of leaf size. Science 357, 917-921.
| Crossref | Google Scholar | PubMed |
